Chia-Min Hsu

Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas

In the context of rising seawater temperatures associated with climate change,  the issue of whether coral holobionts deal with this challenge by shuffling their associations with stress‐ and/or heat‐tolerant Symbiodinium, by generating heat‐resistant host genotypes, or both is important for coral survival. In this study, the composition of communities of the endosymbiont Symbiodinium and the population genetics of the coral host Platygyra verweyi were examined in a reef impacted by hot‐water discharged from the outlet of a nuclear power plant in operation in Kenting, Southern Taiwan since 1984. The water at this site is 2.0–3.0 °C warmer than adjacent reefs in summer, which have an average seawater temperature of 29.0 °C. The data were compared with those for the same species at other sites within 12 km of the outlet site. Platygyra verwyei was associated with one or both of Symbiodinium types C3 (heat sensitive) and D1a (heat tolerant) at all sites with the latter being the dominant at the nuclear power plant outlet. The proportion of C3 in populations increased gradually with increasing distance from the hot‐water discharge. Genetic analysis of the Platygyra verweyi host using mitochondrial and nuclear markers showed no genetic differentiation among sites. Changes in the composition of Symbiodinium types associated with P. verweyi among closely located sites in Kenting suggested that this coral might have acclimatized to the constant thermal stress by selective association with heat‐tolerant Symbiodinium types, whereas the role of the host in adaptation was inconclusive.

Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input

Climate change has led to a decline in the health of corals and coral reefs around the world. Studies have shown that, while some corals can cope with natural and anthropogenic stressors either through resistance mechanisms of coral hosts or through sustainable relationships with Symbiodinium clades or types, many coral species cannot. Here, we show that the corals present in a reef in southern Taiwan, and exposed to long-term elevated seawater temperatures due to the presence of a nuclear power plant outlet (NPP OL), are unique in terms of species and associated Symbiodinium types. At shallow depths (<3 m), eleven coral genera elsewhere in Kenting predominantly found with Symbiodinium types C1 and C3 (stress sensitive) were instead hosting Symbiodinium type D1a (stress tolerant) or a mixture of Symbiodinium type C1/C3/C21a/C15 and Symbiodinium type D1a. Of the 16 coral genera that dominate the local reefs, two that are apparently unable to associate with Symbiodinium type D1a are not present at NPP OL at depths of <3 m. Two other genera present at NPP OL and other locations host a specific type of Symbiodinium type C15. These data imply that coral assemblages may have the capacity to maintain their presence at the generic level against long-term disturbances such as elevated seawater temperatures by acclimatization through successful association with a stress-tolerant Symbiodinium over time. However, at the community level it comes at the cost of some coral genera being lost, suggesting that species unable to associate with a stress-tolerant Symbiodinium are likely to become extinct locally and unfavorable shifts in coral communities are likely to occur under the impact of climate change.

Identification of scleractinian coral recruits using fluorescent censusing and DNA barcoding techniques.

The identification of coral recruits has been problematic due to a lack of definitive morphological characters being available for higher taxonomic resolution. In this study, we tested whether fluorescent detection of coral recruits used in combinations of different DNA-barcoding markers (cytochrome oxidase I gene [COI], open reading frame [ORF], and nuclear Pax-C intron [PaxC]) could be useful for increasing the resolution of coral spat identification in ecological studies. One hundred and fifty settlement plates were emplaced at nine sites on the fringing reefs of Kenting National Park in southern Taiwan between April 2011 and September 2012. A total of 248 living coral spats and juveniles (with basal areas ranging from 0.21 to 134.57 mm2) were detected on the plates with the aid of fluorescent light and collected for molecular analyses. Using the COI DNA barcoding technique, 90.3% (224/248) of coral spats were successfully identified into six genera, including Acropora, Isopora, Montipora, Pocillopora, Porites, and Pavona. PaxC further separated I. cuneata and I. palifera of Isopora from Acropora, and ORF successfully identified the species of Pocillopora (except P. meandrina and P. eydouxi). Moreover, other cnidarian species such as actinarians, zoanthids, and Millepora species were visually found using fluorescence and identified by COI DNA barcoding. This combination of existing approaches greatly improved the taxonomic resolution of early coral life stages, which to date has been mainly limited to the family level based on skeletal identification. Overall, this study suggests important improvements for the identification of coral recruits in ecological studies.

Wall of orange cup coral, Tubastraea coccinea, at the inlet breakwaters of a nuclear power plant, southern Taiwan

The Indo-Pacific reef coral Tubastraea coccinea Lesson, 1829, is a highly competitive invasive species, which has spread over the tropical West Atlantic after its introduction at Puerto Rico and Curaçao during the late 1930s (Cairns 2000; Fenner and Banks 2004; Riul et al. 2013). Here it colonizes hard substrates along rocky shores, including oil platforms, ship hulls, and the undersides of boulders, where it is causing damage to native reef-building coral species and structure modification of benthic communities (Lages et al. 2010). However, the capacity of T. coccinea to expand and to form dense aggregations on artificial substrates is not yet known from the Indo-Pacific, since most reports described its natural habitat as the cryptic reefs, where zooxanthellate corals are absent (Sammarco et al. 2014). In July, 2015, we discovered a benthic community dominated by T. coccinea (Fig. 1a) growing on a vertical concrete wall adjacent to the turbines of the inlet (IL) in the third nuclear power plant (NPP), the Kenting National Park, Taiwan (21°57′20.3′′N 120°45′13.5′′E). The breakwaters of the NPP-IL (1–6 m deep) was covered by dense zooxanthellate corals, where 25 Acropora species were recorded and represented over 56 % of Acropora species diversity described in Taiwan (Tang et al. 2010). In contrast, T. coccinea (an azooxanthellate coral) occupied the wall with relatively high densities (mean: 51.6 colonies m, measured by nine 0.5 × 0.5-m quadrats). The colony size of T. coccinea on the wall was relatively large with colony surface area ranging from 46.6 to 673.6 cm (n = 10). In addition, two other Tubastraea species, T. faulkneri and T. micranthus, were found sporadically on the same wall (Fig. 1b, c). The density and colony size of T. coccinea found in the NPP-IL are comparable to those described from oil platforms in the northern Gulf of Mexico (Sammarco et al. 2014), suggesting that T. coccinea has a similar ability to colonize artificial structures in the Indo-Pacific as its conspecifics in the Atlantic. Communicated by B. W. Hoeksema

High coral cover and subsequent high fish richness on mature breakwaters in Taiwan

Breakwaters are widely used in coastal development. Breakwaters can alter habitats by undermining shallow coastal ecosystems, especially coral reefs. However, recent studies indicate that mature breakwaters can have well-developed corals and coral-associated fishes. Breakwaters with colonized corals may act as surrogates of natural coral reefs against the global coral crisis. Here, we examined the composition of corals, fishes, and benthic biota/abiota between natural reefs and mature breakwaters to evaluate the possibility of breakwaters supplementing natural reefs. We found equal or higher coral cover, fish abundance, and species richness on breakwaters. Conversely, differential coral growth forms and fish assemblages on mature breakwaters suggested the irreplaceability of natural reefs. Corals and coral reef fishes on mature man-made structures, however, may improve the resistance and resilience of coral reefs. Conclusively, despite high coral cover on mature man-made structures appropriate management (e.g., marine reserves) is still necessary to sustain the coral reefs.

Larval release and rapid settlement of the coral-killing sponge, Terpios hoshinota, at Green Island, Taiwan

Since the description of Terpios hoshinota from Guam (Rutzler and Muzik 1993), there have been recent reports of increased incidences of invasion by this coralkilling cyanobacteriosponge on Indo-Pacific coral reefs (Fujii et al. 2011; de Voogd et al. 2013). However, the life-history strategy behind its invasive capacity remains unknown. In November 2010, at full moon, Acropora sp. branches overgrown by T. hoshinota were collected from Daibaisha reef (22°38′20.05′′N, 121°29′31.05′′E), at Green Island, Taiwan. Six hours after collection, parenchymella larvae were observed crawling out from the oscula and remaining on the surface of mother sponges (Fig. 1a, b). A high density of cyanobacteria (∼10/cm) was found in the parenchymella covered with cilia (Wang et al. 2012; Fig. 1c). The larvae rapidly settled and started metamorphosis on substrates consisting of dead coral skeleton and a glass petri dish (Fig. 1d), but not on the surface of live corals (Fig. 1e). These settlement preferences imply that T. hoshinota might not be able to directly attack healthy and live corals, but instead settles on other hard substrates close

Physiological Outperformance at the Morphologically-Transformed Edge of the Cyanobacteriosponge Terpios hoshinota (Suberitidae: Hadromerida) when Confronting Opponent Corals

Terpios hoshinota, an encrusting cyanosponge, is known as a strong substrate competitor of reef-building corals that kills encountered coral by overgrowth. Terpios outbreaks cause significant declines in living coral cover in Indo-Pacific coral reefs, with the damage usually lasting for decades. Recent studies show that there are morphological transformations at a sponge’s growth front when confronting corals. Whether these morphological transformations at coral contacts are involved with physiological outperformance (e.g., higher metabolic activity or nutritional status) over other portions of Terpios remains equivocal. In this study, we compared the indicators of photosynthetic capability and nitrogen status of a sponge-cyanobacteria association at proximal, middle, and distal portions of opponent corals. Terpios tissues in contact with corals displayed significant increases in photosynthetic oxygen production (ca. 61%), the δ13C value (ca. 4%), free proteinogenic amino acid content (ca. 85%), and Gln/Glu ratio (ca. 115%) compared to middle and distal parts of the sponge. In contrast, the maximum quantum yield (Fv/Fm), which is the indicator usually used to represent the integrity of photosystem II, of cyanobacteria photosynthesis was low (0.256~0.319) and showed an inverse trend of higher values in the distal portion of the sponge that might be due to high and variable levels of cyanobacterial phycocyanin. The inconsistent results between photosynthetic oxygen production and Fv/Fm values indicated that maximum quantum yields might not be a suitable indicator to represent the photosynthetic function of the Terpios-cyanobacteria association. Our data conclusively suggest that Terpios hoshinota competes with opponent corals not only by the morphological transformation of the sponge-cyanobacteria association but also by physiological outperformance in accumulating resources for the battle.

Symbiodinium spp. associated with scleractinian corals from Dongsha Atoll (Pratas), Taiwan, in the South China Sea

Dongsha Atoll (also known as Pratas) in Taiwan is the northernmost atoll in the South China Sea and a designated marine national park since 2007. The marine park’s scope of protection covers the bio-resources of its waters in addition to uplands, so it is important to have data logging information and analyses of marine flora and fauna, including their physiology, ecology, and genetics. As part of this effort, we investigated Symbiodinium associations in scleractinian corals from Dongsha Atoll through surveys carried out at two depth ranges (shallow, 1–5 m; and deep, 10–15 m) in 2009 and during a bleaching event in 2010. Symbiodinium composition was assessed using restriction fragment length polymorphism (RFLP) of 28S nuclear large subunit ribosomal DNA (nlsrDNA). Our results showed that the 796 coral samples from seven families and 20 genera collected in 2009 and 132 coral samples from seven families and 12 genera collected in 2010 were associated with Symbiodinium C, D and C+D. Occurrence of clade D in shallow water (24.5%) was higher compared to deep (14.9%). Due to a bleaching event in 2010, up to 80% of coral species associated with Symbiodinium C underwent moderate to severe bleaching. Using the fine resolution technique of denaturing gradient gel electrophoresis (DGGE) of internal transcribed spacer 2 (ITS2) in 175 randomly selected coral samples, from 2009 and 2010, eight Symbiodinium C types and two Symbiodinium D types were detected. This study is the first baseline survey on Symbiodinium associations in the corals of Dongsha Atoll in the South China Sea, and it shows the dominance of Symbiodinium clade C in the population.